Temporal interactions and moon illumination effect on mammals in a tropical semievergreen forest of Manas National Park, Assam, India

3.1 Field sampling design

Mammalian carnivores of varying body size, i.e., large (>20 kg), medium (>10–20 kg), and small (1–10 kg) (Ramesh et al., 2015), and trophic positions (Ritchie & Johnson, 2009) along with their potential prey species (Table S1) were photographed using camera traps in an area of 270 km² within strictly forested habitats of MNP. Camera trap locations were unbaited and selected based on accessibility, terrain features, animal trails, and nallahs (seasonal drainages) with carnivore signs (Marinho et al., 2018; Ramesh et al., 2015). At each location, a single Cuddeback X‐Change™ color model (Cuddeback) with motion sensors and time lag of 1s was set between animal detections. Cameras were fastened to trees at the height of approximately 30–45 cm above the ground for an average of 24 days (range: 16–45). In total, 475 camera trap locations were utilized in a grid‐based approach (grid size: 1 km²) during three sampling periods: April 2017–June 2017 (n = 101), December 2017–May 2018 (n = 154), and November 2018–May 2019 (n = 220) (Figure 1). These months were specifically chosen for greater accessibility and minimal variance in weather conditions. The average temperature and humidity during the entire sampling period were 24°C (±SE 0.29) and 79.4% (±SE 0.54), respectively (http://timeanddate.com).

3.2 Activity periods and activity analysis

4.1 Activity periods

Activity periods for 36 species indicated no sharp boundaries between categories (diurnal, nocturnal, cathemeral, or crepuscular) (Table S2). Small carnivores were found to be either mainly nocturnal (leopard cat and civets) or diurnal (yellow‐throated marten and mongooses). Medium‐sized carnivores (clouded leopard and dhole) were found to be nocturnal or diurnal, and large‐sized carnivores (tiger, leopard, and Asiatic black bear) were cathemeral. Herbivores were either cathemeral (Bos gaurus, Bubalus arnee, and Rusa unicolor) or diurnal (Elephas maximus, Muntiacus muntjak, and Sus scrofa). Terrestrial birds (red junglefowl, Kalij pheasant, Indian peafowl) were found to be diurnal, whereas the routine activity of Indian hare and Himalayan crestless porcupine suggested nocturnal activity.

4.2 Activity pattern and temporal overlaps

4.2.1 Activity overlaps within trophic level

We detected eight small carnivores and evaluated their diel activity pattern (Figure 2). Small carnivores segregated their temporal niche by forming two temporal groups, i.e., nocturnal (leopard cat and civets) and diurnal (yellow‐throated marten and mongooses). Nocturnal small carnivores exhibited high temporal overlap, with the greatest overlap between small Indian civet and Asian palm civet with an overlap coefficient, Δ₄ = 0.92 (95% CI 0.84–0.94); and the MWW test showed significant similarity between their daily distribution of records (W = 1.03, p = 0.6). Similarly, high overlap was also observed between diurnal small carnivores, with the highest coefficient value of Δ₁ = 0.85 (95% CI 0.61–0.88) between crab‐eating mongoose and yellow‐throated marten, and not statistically different (W = 1.50, p = 0.47). However, each diurnal–nocturnal species pairing showed significant differences in circadian activities. All small carnivores followed a bimodal activity pattern except for small Indian mongoose that showed a unimodal activity.

Among large carnivores, tigers and leopards showed the highest daily activity overlap [Δ₄ = 0.87 (95% CI 0.81–0.91)]; however, the MWW test showed significant dissimilarity between their diel activity patterns (W = 23.59, p < 0.01) (Figure 3). Both the species were active throughout the day and night, but leopards were more active during daylight, with peaks in the early morning and late afternoon, whereas tigers were least active from 1,000 to 1500 hr. Two activity peaks (from 1900 to 2300 hr and from 0200 to 0400 hr) were observed for clouded leopards, suggesting a bimodal activity pattern of the species. Dholes showed a unimodal pattern of activity with peaks at 0600 hr. A synchronized least‐active pattern was noted at midnight for clouded leopard, dhole, and Asiatic black bear.

4.2.2 Activity overlaps among trophic level

Among inter‐guild interactions, most small carnivores showed moderate temporal overlap (0.54) with their dominant competitors (Figure 4). However, clouded leopard and dhole had moderately high overlap with nocturnal and diurnal small carnivores, respectively, as they were more active during those phases.

4.2.3 Carnivore and its potential prey

Tigers showed the highest temporal overlap with wild buffalo [Δ₄ = 0.87 (95% CI 0.82–0.92)], sambar (0.86), and gaur (0.79) (Figure 5). In case of leopards, greatest overlap was found with wild buffalo [Δ₄ = 0.81 (95% CI 0.77–0.87)] and gaur (0.81), whereas clouded leopards had maximum overlap with Himalayan crestless porcupine [Δ₁ = 0.77 (95% CI 0.58–0.87)] and barking deer (0.49). High temporal overlap was found among diurnal prey species such as barking deer [Δ₄ = 0.65 (95% CI 0.61–0.74)] and wild boar (0.63) with dholes, whereas Indian hares were active during night time and showed high overlap with leopard cats. MWW test showed similar activity between tiger and wild buffalo (W = 1.20, p = 0.55), clouded leopard and Himalayan crestless porcupine (W = 5.59, p = 0.06), and leopard cat and Indian hare (W = 4.13, p = 0.13).

4.2.4 Moon phase

The activity patterns of mammals were correlated with different moon phases, with the greatest records of large carnivore (n = 939), large prey (n = 21,212), and small prey (n = 92) captured in the full moon, whereas civets (n = 932) and small felid (n = 377) had more photographs during the new moon (Figure 6, Figure S1).

One‐way ANOVA result indicated significant variance for all the species guild except for large carnivores (Table S3). Dunn–Sidak test showed significantly more records for civets during the new moon (mean differences = 2.92, p < 0.005) than in the full moon. More records of large prey were recorded during the full moon (mean differences = 7.3, p < 0.05) than in the new moon.

The results of partial correlation depicted a negative relation between civets and moon visible surface while controlling for large carnivores (r = −0.45, p < 0.05) (Table S4). Bivariate correlation also showed a negative correlation between them (r = −0.44, p < 0.01) (Table S5). Large prey (r = 0.15, p < 0.05) and small prey (r = 0.13, p < 0.05) showed positive correlation with the moon visible surface.

Results of circular statistics were also in line with the above results (Figure 7, Table 1). Civet activity was not uniform during the lunar cycle (U = 333.83, p < 0.01) and was statistically more likely around the new moon (μ = 23.99°, r = 0.45). Large carnivore (μ = 152.86°), large prey (μ = 131.35°), and small prey (μ = 133.23°) were more likely to be active around waxing gibbous and full moon, whereas small felid (μ = 80.55°) records were highest just before the first quarter.

TABLE 1. Linear–circular association (mean vector, length of mean vector, and Rao's spacing test) between the activity of mammals and lunar cycle

	Mean vector	Length of mean vector		Rao's spacing test
	μ	r	p	U
Large Carnivore	152.86°	0.08	0.11	313.87*
Large prey	131.35°	0.20	<0.001	357.20*
Civets	23.99°	0.45	<0.001	333.83*
Small felid	80.55°	0.16	<0.001	294.12*
Small prey	133.23°	0.17	<0.001	214.32*

Note

• The non‐random distribution (p < .01) was indicated with an asterisk (*).

5.1 Activity periods

van Schaik and Griffiths (1996) suggest that smaller mammals (<10 kg) tend to be specifically nocturnal or diurnal as an anti‐predation strategy, whereas larger mammals (>10 kg) are more cathemeral because of energy requirements and associated feeding commitments. In this study also, all recorded small‐ and medium‐sized mammals were found to be mainly nocturnal or diurnal and larger‐sized mammals were found to be active during both day and night hours.

5.2 Activity patterns and temporal overlaps

We found differences in tiger and leopard activity peaks, but significant time overlap between them was evident. They avoid competition by hunting with different activities and in different vegetation strata, as well as on different prey species (Seidensticker, 1976). Tigers may use wide and established trails for movement (Kawanishi, 2002), but leopards may avoid them by using smaller trails or different activity patterns. Our study showed considerably higher activity overlaps (>0.50) of tigers with medium‐ to large‐sized prey (Hayward et al., 2012) and leopards with small–medium‐ to large‐sized prey (Hayward et al., 2006). Leopard activity was diurnal (51%) in tandem with medium‐sized prey, i.e., barking deer and wild boar (Hayward et al., 2006). Asiatic black bear was diurnal (Hwang & Garshelis, 2007) or crepuscular (Sharma et al., 2010); however, our study highlighted a cathemeral pattern.

The study showed that clouded leopard activity was predominantly nocturnal (Adul et al., 2015; Azlan & Sharma, 2006; Grassman et al., 2005a; Mukherjee et al., 2019) with bimodal peaks at 1900–2300 hr and 0200–0400 hr. Although overall radiotelemetry studies reported distinct activity peaks in the morning followed by evening crepuscular hours (Austin et al., 2010; Grassman et al., 2005a). We expected low temporal overlap of clouded leopards with tigers and leopards due to the risk of interspecific killing of clouded leopards by both top predators. However, contrary to our expectations, the temporal overlap (>0.70) was relatively high. We believe that clouded leopards may be able to avoid tigers and leopards by exhibiting arboreal behavior when they encounter them (Austin ,2002) or by selecting different prey species (Ngoprasert et al., 2012). The stocky build, large canines, and the large postcanine space make clouded leopards capable of killing relatively large prey (Therrien, 2005). However, our study reported high overlap with small‐ (Himalayan crestless porcupine) to medium‐sized prey (barking deer). Clouded leopard terrestrial activity was found to be less during daytime (n = 2), a behavior predicted for areas that have top predators (van Schaik & Griffiths, 1996). The low capture rate of 21 photographs in 11,294 trap nights in our study does not necessarily reflect low numbers of the felid but rather decreased probability captures along wildlife trails and roads that were frequented by high numbers of tigers and leopards.

Dhole, the only canid species recorded during the study, showed diurnal activity with bimodal peaks, i.e., morning and evening. Their activity was found to be segregated temporarily with dominant competitors (tigers and leopards), similar to most studies in India and Southeast Asia (Grassman et al., 2005b; Jenks et al., 2012; Khoewsree et al., 2020; Singh & Macdonald, 2017; Sukmasuang et al., 2020). However, Nurvianto et al. (2015) and Ghaskadbi et al. (2016) observed a crepuscular activity. The dhole diet includes a wide variety of prey species, ranging from small rodents and hares to gaur (Hayward et al., 2014; Selvan et al., 2013a, b). Their hunting success varies depending on the pack size, prey species, and habitat (Acharya ,2007; Johnsingh, 1983). In tropical semievergreen forests, the species appear to persist in smaller packs and consume medium‐sized prey (Kawanishi & Sunquist, 2008), as smaller packs are more energetically advantageous in the rainforest where large prey species are scarce. Thick vegetation also favors stalk and ambush hunting techniques over cursorial hunting, and competition with tigers and leopards for small‐ to medium‐sized prey is high (Kawanishi & Sunquist, 2004). It was evident that the predator's activity was driven primarily by prey activity; hence, dholes showed high temporal overlap with medium‐sized diurnal prey, such as barking deer and wild boar (Khoewsree et al., 2020; Sukmasuang et al., 2020).

The only small felid to be recorded as strictly nocturnal was leopard cat, which was consistent with other reported studies (Can et al., 2020; Chen et al., 2016; Lynam et al., 2013; Mukherjee et al., 2019). However, few studies contradict the nocturnality of leopard cats (Azlan & Sharma, 2006; Grassman et al., 2005c; Saxena & Rajvanshi, 2014). Civets were active during nocturnal hours, similar to other reported studies (Sukmasuang et al., 2020; Than et al., 2008), although a study of Azlan (2003) suggests crepuscular activity. Mongooses and yellow‐throated marten were documented as diurnal (Sukmasuang et al., 2020; Zhao et al., 2020); however, Prater & Barruel (1971) and Santiapillai et al. (2000) observed cathemeral activity. The emergence of diurnal and nocturnal groups of small carnivores, a finding reflected at both broad and fine temporal scales, is a reflection of such a partitioning strategy. The Himalayan crestless porcupine was nocturnal, consistent with previous studies by Menon (2003) and Ampeng et al. (2018). Indian hare was predominantly active during crepuscular and nocturnal hours (Molur et al., 2005); however, we reported only nocturnal activity. According to Harmsen et al. (2011), the diel activity of many felids is associated with the activity pattern of their prey. The main reason small cats were nocturnal in the study area could be that rodents and hares, their primary prey, were generally nocturnal (Mukherjee et al., 2016; Xiong et al., 2017), although we could not quantify this through camera trapping.

Smaller carnivores may reduce risk of encountering larger carnivores by temporarily avoiding them. Our study showed that small carnivores separated their temporal axis by forming distinct coexistence groups, i.e., diurnal and nocturnal, and exhibited low temporal overlaps with dominant predators. Among competitors, the difference in body size is likely to trigger behavioral avoidance in subordinate species to avoid interspecific or exploitative competition (Lucherini et al., 2009). Fedriani et al. (2000) found that coyotes (Canis latrans), the largest predator, utilized various habitats and food types and practiced interspecific killing of smaller competitors, thus limiting the distribution of grey foxes (Urocyon cinereoargenteus) and bobcats (Felis rufus). Indeed, body size is important in driving coexistence patterns and suggests that similar dynamics may exist among the small carnivores in our study.

Our results support that temporal segregation facilitates the coexistence of carnivore community in a tropical region, suggesting a partial avoidance that may decrease competition as well as the risk of intraguild predation (Carothers and Jaksić, 1984). Although most species pairs in the large carnivore guild exhibited a high overlap, almost all carnivores segregated at least their activity peaks. However, small carnivores exploited different temporal niches. Results also support the dominant competitor avoidance hypothesis. The high temporal overlap among predator–prey might be the result of predators’ effort to synchronize their activities with those of their potential prey species, supporting the prey synchrony hypothesis.

5.3 Do species respond differently to moonlight?

Moonlight has usually been thought to increase predation risk by enhancing the ability of predators to detect prey (Kotler et al., 1991; Nash, 2007), leading to decreased activity or shifts in prey foraging efficiency in brighter nights (Daly et al., 1992; Orrock et al., 2004; Prugh & Golden, 2014). Both increasing activity under brighter conditions, as well as increasing activity under darker conditions, have been interpreted as anti‐predator strategies in mammals. Brighter nights may help prey spot approaching predators, while dark conditions may allow them to remain undetected by their predators.

The results across 17 lunar cycles suggested that large carnivores (r = 0.08) were active non‐differentially across the lunar cycles, and their activity reached its peak every 4–5 days, followed by a gradual decrease. Moonlight strongly influenced the foraging patterns of prey species. Both large‐ and small‐sized prey activities were found to be more during the full moon nights, suggesting that the full moon could increase their visual efficiency in detecting and avoiding predators (Clarke, 1983; Griffin et al., 2005). This anti‐predator behavior is already well recognized for marsupials and rodents (Bitetti et al., 2006; de Matos Dias et al., 2018). Civets mainly use tactile, olfactory, and aural senses while foraging (Mudappa 2013), and their activity is found less during brighter nights (Ampeng et al., 2018; Grassman et al., 2005d). We also found that moonlight negatively influenced civet activity, and their activity decreases with increasing moonlight intensity. Civets were more active during darker nights, possibly to avoid dominant predators and perhaps to increase foraging efficiency.

The moonlight results partially support the dominant predator avoidance hypothesis, while prey species are found to be more active during brighter nights to locate food and predators according to the visual acuity hypothesis (Prugh & Golden, 2014).